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ABSTRACT Over six decades of research on wild baboons and their close relatives (collectively, the African papionins) has uncovered substantial variation in their behavior and social organization. While most papionins form discrete social groups (single-level societies), a few others form small social units nested within larger aggregations (multi-level societies). To understand the social processes that shape this variation, a more systematic, comparative analysis of social structure is needed. Here, we constructed a database of behavioral and demographic records spanning 135 group-years across 13 long-term papionin field studies to (i) quantify variation in grooming network structure, and (ii) identify the factors (e.g., sex, kinship, and social status effects) that underlie these differences. We detected considerable variation in grooming network structure across the papionins, even within the classic single-level societies. The papionins could be best divided into three broad categories: single-levelcohesive, single-levelcliquish, andmulti-level. The cohesive single-level societies formed networks that were dense, moderately kin-biased, and weakly rank-structured, while the cliquish single-level societies formed networks that were relatively modular, highly kin-biased, and more strongly rank-structured. As expected, multi-level networks were highly modular and shaped by females’ ties to specific dominant males but varied in their kin biases. Taken together, these data suggest that: (i) discrete typologies obscure variation in social structure; and (ii) similarities in social structure are sometimes, but not always, shaped by similar social processes. SIGNIFICANCE STATEMENTDo all primate groups fit the same social mold? While factors like kinship and dominance shape the social lives of many of our close relatives, it remains unclear how their effects differ across species. Using a new database representing decades of field research, we found that baboons and their close relatives fell into one of three general patterns: one in which groups were cohesive and only somewhat nepotistic (i.e., kin- and rank-biased), another in which groups were more cliquish and nepotistic, and a final pattern in which groups were divided into clusters centered on dominant males. Distinct primate societies may thus reflect differences in the strength of females’ social biases towards kin and the degree of males’ social influence. 

Abstract Female reproductive maturation is a critical life-history milestone, initiating an individual’s reproductive career. Studies in social mammals have often focused on how variables related to nutrition influence maturation age in females. However, parallel investigations have identified conspicuous male-mediated effects in which female maturation is sensitive to the presence and relatedness of males. Here, we evaluated whether the more “classic” socioecological variables (i.e., maternal rank, group size) predict maturation age in wild geladas—a primate species with known male-mediated effects on maturation and a grassy diet that is not expected to generate intense female competition. Females delayed maturation in the presence of their fathers and quickly matured when unrelated, dominant males arrived. Controlling for these male effects, however, higher-ranking daughters matured at earlier ages than lower-ranking daughters, suggesting an effect of within-group contest competition. However, contrary to predictions related to within-group scramble competition, females matured earliest in larger groups. We attribute this result to either: 1) a shift to “faster” development in response to the high infant mortality risk posed by larger groups; or 2) accelerated maturation triggered by brief, unobserved male visits. While earlier ages at maturation were indeed associated with earlier ages at first birth, these benefits were occasionally offset by male takeovers, which can delay successful reproduction via spontaneous abortion. In sum, rank-related effects on reproduction can still occur even when socioecological theory would predict otherwise, and males (and the risks they pose) may prompt female maturation even outside of successful takeovers. 

Abstract Neopterin, a product of activated white blood cells, is a marker of nonspecific inflammation that can capture variation in immune investment or disease-related immune activity and can be collected noninvasively in urine. Mounting studies in wildlife point to lifetime patterns in neopterin related to immune development, aging, and certain diseases, but rarely are studies able to assess whether neopterin can capture multiple concurrent dimensions of health and disease in a single system. We assessed the relationship between urinary neopterin stored on filter paper and multiple metrics of health and disease in wild geladas (Theropithecus gelada), primates endemic to the Ethiopian highlands. We tested whether neopterin captures age-related variation in inflammation arising from developing immunity in infancy and chronic inflammation in old age, inflammation related to intramuscular tapeworm infection, helminth-induced anti-inflammatory immunomodulation, and perturbations in the gastrointestinal microbiome. We found that neopterin had a U-shaped relationship with age, no association with larval tapeworm infection, a negative relationship with metrics related to gastrointestinal helminth infection, and a negative relationship with microbial diversity. Together with growing research on neopterin and specific diseases, our results demonstrate that urinary neopterin can be a powerful tool for assessing multiple dimensions of health and disease in wildlife. 

Abstract Background Adaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments. Results Here, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas ( Theropithecus gelada ). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods. Conclusion Together, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa.